Proper central nervous system (CNS) function in vertebrates and invertebrates alike requires the sufficient production of, and suitable interaction between, different classes of neurons and glial cells. Although a large heterogeneity exists between individual cells of the CNS, one can begin dissecting its construction, and ultimately function, based on developmental principles. One such principle is the lineage concept; accumulating evidence suggests that in the CNS of the fruit fly Drosophila melanogaster, classes of cells can be defined based on their progenitor origin, or lineage. Neurons and/or glial cells which derive from an individual progenitor, of which there are approximately 100 per brain hemisphere, exhibit common structural properties. In this dissertation we describe the lineage relationship, and resultant characteristics, of Drosophila brain cells in two contexts: glial cells populating the neuropil-cortex interface (neuropil glia) and ensembles of neurons transmitting visual information to a higher-order brain region called the central complex (Anterior Visual Pathway). In the first context, we find that astrocyte-like glial cells (ALGs), a neuropil glia subtype reminiscent of vertebrate astrocytes, are generated in two distinct waves. The first wave results from the proliferation of embryonic progenitors in the basal brain, and produces the mature ALGs of the larval brain. ALGs of the adult brain, produced during the second wave, are generated from a completely separate population of progenitors in the larva. We also characterize the cytology of these glial populations. In the second context, we find that all ring neurons of the ellipsoid body, a subcompartment of the central complex, are generated from a single lineage called DALv2. Ring neurons are a peculiar neuronal class which has been previously shown to respond to visual stimuli and are required for higher-order visually-guided behaviors. We identify two further lineages, DALcl1 and 2, which generate parallel ensembles of neurons providing visual input to ring neurons. Importantly, neurons of DALcl1 and 2 are not only developmentally-distinct, but also exhibit structural and functional differences, highlighting the rarely demonstrated principle that functional neuronal circuitry can be mapped to developmental cell lineage. Taken together, this thesis validates the utility of employing the lineage principle to formulate hypotheses of circuit function and nervous system assembly in general.